Impact of hemlock woolly adelgid (Adelges tsugae) infestation on xylem structure and function and leaf physiology in eastern hemlock (Tsuga canadensis)
Brett A. Huggett A F , Jessica A. Savage B C , Guang-You Hao D , Evan L. Preisser E and N. Michele Holbrook B
+ Author Affiliations
- Author Affiliations
A Biology Department, Bates College, Lewiston, ME 04240, USA.
B Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA.
C Department of Biology, University of Minnesota, Duluth, MN 55812, USA.
D CAS Key Laboratory of Forest Ecology and Management, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, 110016, China.
E Biological Sciences, University of Rhode Island, Kingston, RI 02881, USA.
F Corresponding author. Email: bhuggett@bates.edu
Functional Plant Biology 45(5) 501-508 https://doi.org/10.1071/FP17233
Submitted: 14 August 2017 Accepted: 1 November 2017 Published: 18 December 2017
Abstract
Hemlock woolly adelgid (Adelges tsugae Annand) (HWA) is an invasive insect that feeds upon the foliage of eastern hemlock (Tsuga canadensis (L.) Carrière) trees, leading to a decline in health and often mortality. The exact mechanism leading to the demise of eastern hemlocks remains uncertain because little is known about how HWA infestation directly alters the host’s physiology. To evaluate the physiological responses of eastern hemlock during early infestation of HWA, we measured needle loss, xylem hydraulic conductivity, vulnerability to cavitation, tracheid anatomy, leaf-level gas exchange, leaf water potential and foliar cation and nutrient levels on HWA-infested and noninfested even-aged trees in an experimental garden. HWA infestation resulted in higher xylem hydraulic conductivity correlated with an increase in average tracheid lumen area and no difference in vulnerability to cavitation, indicating that needle loss associated with HWA infestation could not be attributed to reduced xylem transport capacity. HWA-infested trees exhibited higher rates of net photosynthesis and significant changes in foliar nutrient partitioning, but showed no differences in branch increment growth rates compared with noninfested trees. This study suggests that HWA-induced decline in the health of eastern hemlock trees is not initially caused by compromised water relations or needle loss.
Additional keywords: cavitation, foliar cations, hydraulic conductivity, photosynthesis.
References
Alder NN, Pockman WT, Sperry JS, Nuismer S (1997) Use of centrifugal force in the study of xylem cavitation. Journal of Experimental Botany 48, 665–674.| Use of centrifugal force in the study of xylem cavitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjs1Kltb0%3D&md5=cbb31e880500b83da57ff014772e7771CAS |
Cherubini P, Gartner BL, Tognetti R, Bräker O, Schoch W, Innes JL (2003) Identification, measurement and interpretation of tree rings in woody species from Mediterranean climates. Biological Reviews of the Cambridge Philosophical Society 78, 119–148.
| Identification, measurement and interpretation of tree rings in woody species from Mediterranean climates.Crossref | GoogleScholarGoogle Scholar |
Copenheaver CA, Pokorski EA, Currie JE, Abrams MD (2006) Causation of false ring formation in Pinus banksiana: a comparison of age, canopy class, climate and growth rate. Forest Ecology and Management 236, 348–355.
| Causation of false ring formation in Pinus banksiana: a comparison of age, canopy class, climate and growth rate.Crossref | GoogleScholarGoogle Scholar |
Domec JC, Rivera LN, King JS, Peszlen I, Hain F, Smith B, Frampton J (2013) Hemlock woolly adelgid (Adelges tsugae) infestation affects water and carbon relations of eastern hemlock (Tsuga canadensis) and Carolina hemlock (Tsuga caroliniana). New Phytologist 199, 452–463.
| Hemlock woolly adelgid (Adelges tsugae) infestation affects water and carbon relations of eastern hemlock (Tsuga canadensis) and Carolina hemlock (Tsuga caroliniana).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpvFars7w%3D&md5=1c82fb6bd72219f441066e98cb2aab7dCAS |
Ewers FW, Zimmermann MH (1984) The hydraulic architecture of eastern hemlock (Tsuga canadensis). Canadian Journal of Botany 62, 940–946.
| The hydraulic architecture of eastern hemlock (Tsuga canadensis).Crossref | GoogleScholarGoogle Scholar |
Eyles A, Smith D, Pinkard EA, Smith I, Corkrey R, Elms S, Beadle C, Mohammed C (2011) Photosynthetic responses of field-grown Pinus radiata trees to artificial and aphid-induced defoliation. Tree Physiology 31, 592–603.
| Photosynthetic responses of field-grown Pinus radiata trees to artificial and aphid-induced defoliation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFGns7zL&md5=aa9037d8046bd8647945be527e6514faCAS |
Gómez S, Orians CM, Preisser EL (2012) Exotic herbivores on a shared native host: tissue quality after individual, simultaneous, and sequential attack. Oecologia 169, 1015–1024.
| Exotic herbivores on a shared native host: tissue quality after individual, simultaneous, and sequential attack.Crossref | GoogleScholarGoogle Scholar |
Gómez S, Gonda-King L, Orians C, Orwig D, Panko R, Radville L, Soltis N, Thornber C, Preisser E (2015) Interactions between invasive herbivores and their long-term impact on New England hemlock forests. Biological Invasions 17, 661–673.
| Interactions between invasive herbivores and their long-term impact on New England hemlock forests.Crossref | GoogleScholarGoogle Scholar |
Gonda-King L, Radville L, Preisser EL (2012) False ring formation in eastern hemlock branches: impacts of hemlock woolly adelgid and elongate hemlock scale. Environmental Entomology 41, 523–531.
| False ring formation in eastern hemlock branches: impacts of hemlock woolly adelgid and elongate hemlock scale.Crossref | GoogleScholarGoogle Scholar |
Gonda-King L, Gómez S, Martin JL, Orians CM, Preisser EL (2014) Tree responses to an invasive sap-feeding insect. Plant Ecology 215, 297–304.
| Tree responses to an invasive sap-feeding insect.Crossref | GoogleScholarGoogle Scholar |
Hollingsworth RG, Hain FP (1992) Balsam woolly adelgid (Homoptera: Adelgidae) and spruce-fir decline in the southern Appalachians: assessing pest relevance in a damaged ecosystem. Functional Ecology 74, 179–187.
Jansen S, Choat B (2011) ‘Making wood anatomical measurements with imageJ.’ Available at http://prometheuswiki.org/tiki-index.php?page=Making+wood+anatomical+measurements+with+imageJ [Verified November 2017].
Långström B, Hellqvist C, Cedervind J (2004) Comparison of methods for estimation of needle losses in Scots pine following defoliation by Bupalus piniaria. Silva Fennica 38, 15–27.
| Comparison of methods for estimation of needle losses in Scots pine following defoliation by Bupalus piniaria.Crossref | GoogleScholarGoogle Scholar |
Marschner H (1995) ‘Mineral nutrition of higher plants.’ (Academic Press: London).
Mayr S, Cochard H (2003) A new method for vulnerability analysis of small xylem areas reveals that compression wood of Norway spruce has lower hydraulic safety than opposite wood. Plant, Cell & Environment 26, 1365–1371.
| A new method for vulnerability analysis of small xylem areas reveals that compression wood of Norway spruce has lower hydraulic safety than opposite wood.Crossref | GoogleScholarGoogle Scholar |
McClure MS (1991) Density-dependent feedback and population cycles in Adelges tsugae (Homoptera: Adelgidae) on Tsuga canadensis. Environmental Entomology 20, 258–264.
| Density-dependent feedback and population cycles in Adelges tsugae (Homoptera: Adelgidae) on Tsuga canadensis.Crossref | GoogleScholarGoogle Scholar |
Miflin BJ, Habash DZ (2002) The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops. Journal of Experimental Botany 53, 979–987.
| The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XivFSnur8%3D&md5=4dbdd2d131ae8daf1cae5bc2e5a656b6CAS |
Miller-Pierce MR, Preisser EL (2012) Asymmetric priority effects influence the success of invasive forest insects. Ecological Entomology 37, 350–358.
| Asymmetric priority effects influence the success of invasive forest insects.Crossref | GoogleScholarGoogle Scholar |
Miller-Pierce MR, Orwig DA, Preisser E (2010) Effects of hemlock woolly adelgid and elongate hemlock scale on eastern hemlock growth and foliar chemistry. Environmental Entomology 39, 513–519.
| Effects of hemlock woolly adelgid and elongate hemlock scale on eastern hemlock growth and foliar chemistry.Crossref | GoogleScholarGoogle Scholar |
Nuckolls AE, Wurzburger N, Ford CR, Hendrick RL, Vose JM, Kloeppel BD (2009) Hemlock declines rapidly with hemlock woolly adelgid infestation: impacts on the carbon cycle of southern Appalachian forests. Ecosystems 12, 179–190.
| Hemlock declines rapidly with hemlock woolly adelgid infestation: impacts on the carbon cycle of southern Appalachian forests.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisVCrt74%3D&md5=6dacdca26befe5694cfa8af2a5bb8d72CAS |
Orwig DA, Foster D, Mausel D (2002) Landscape patterns of hemlock decline in New England due to the introduced hemlock woolly adelgid. Journal of Biogeography 29, 1475–1487.
| Landscape patterns of hemlock decline in New England due to the introduced hemlock woolly adelgid.Crossref | GoogleScholarGoogle Scholar |
Orwig DA, Barker Plotkin A, Davidson E, Lux H, Savage K, Ellison A (2013) Foundation species loss affects vegetation structure more than ecosystem function in a northeastern USA forest. PeerJ 1, e41
| Foundation species loss affects vegetation structure more than ecosystem function in a northeastern USA forest.Crossref | GoogleScholarGoogle Scholar |
Paradis AF (2011) ‘Population dynamics of the hemlock woolly adelgid (Hemiptera: Adelgidae).’ (University of Massachusetts, Amherst)
Pontius JA, Hallett RA, Jenkins JC (2006) Foliar chemistry linked to infestation and susceptibility to hemlock woolly adelgid (Homoptera: Adelgidae). Environmental Entomology 35, 112–120.
| Foliar chemistry linked to infestation and susceptibility to hemlock woolly adelgid (Homoptera: Adelgidae).Crossref | GoogleScholarGoogle Scholar |
Radville L, Chaves A, Preisser EL (2011) Variation in plant defense against invasive herbivores: evidence for a hypersensitive response in eastern hemlocks (Tsuga canadensis). Journal of Chemical Ecology 37, 592–597.
| Variation in plant defense against invasive herbivores: evidence for a hypersensitive response in eastern hemlocks (Tsuga canadensis).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXntFGmsrk%3D&md5=f70f086ee1641cb7cda4c7102461d55fCAS |
Rhodes D, Verslues PE, Sharp RE (1999) Role of amino acids in abiotic stress resistance. In ‘Plant amino acids. Biochemistry and biotechnology’. (Ed. BK Singh.) pp. 319–356. (Marcel Dekker: New York)
Rosner S, Klein A, Müller U, Karlsson B (2007) Hydraulic and mechanical properties of young Norway spruce clones related to growth and wood structure. Tree Physiology 27, 1165–1178.
| Hydraulic and mechanical properties of young Norway spruce clones related to growth and wood structure.Crossref | GoogleScholarGoogle Scholar |
Rossi S, Simard S, Deslauriers A, Morin H (2009) Wood formation in Abies balsamea seedlings subjected to artificial defoliation. Tree Physiology 29, 551–558.
| Wood formation in Abies balsamea seedlings subjected to artificial defoliation.Crossref | GoogleScholarGoogle Scholar |
Rubino L, Charles S, Sirulnik AG, Tuininga AR, Lewis JD (2015) Invasive insect effects on nitrogen cycling and host physiology are not tightly linked. Tree Physiology 35, 124–133.
| Invasive insect effects on nitrogen cycling and host physiology are not tightly linked.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXnvFShsbk%3D&md5=61a86fe1ee418a294078182aba971e38CAS |
Salleo S, Nardini A, Raimondo F, Assunta M, Gullo L, Pace F (2003) Effects of defoliation caused by the leaf miner Cameraria ohridella on wood production and efficiency in Aesculus hippocastanum growing in north-eastern Italy. Trees 17, 367–375.
Scholander PF, Hammel HT, Bradstreet ED, Hemmingsen EA (1965) Sap pressure in vascular plants: negative hydrostatic pressure can be measured in plants. Science 148, 339–346.
| Sap pressure in vascular plants: negative hydrostatic pressure can be measured in plants.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cvlsVKquw%3D%3D&md5=4a71e1fc892d77d3e35ed972c2754a3eCAS |
Scholz A, Klepsch M, Karimi Z, Jansen S (2013) How to quantify conduits in wood? Frontiers in Plant Science 4, 56
| How to quantify conduits in wood?Crossref | GoogleScholarGoogle Scholar |
Soltis NE, Gómez S, Leisk GG, Sherwood P, Preisser EL, Bonello P, Orians CM (2014) Failure under stress: the effect of the exotic herbivore Adelges tsugae on biomechanics of Tsuga canadensis. Annals of Botany 113, 721–730.
| Failure under stress: the effect of the exotic herbivore Adelges tsugae on biomechanics of Tsuga canadensis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjsFGhu7k%3D&md5=3f65e0771205869a6f38072572481436CAS |
Soltis NE, Gómez S, Gonda‐King L, Preisser EL, Orians CM (2015) Contrasting effects of two exotic invasive hemipterans on whole‐plant resource allocation in a declining conifer. Entomologia Experimentalis et Applicata 157, 86–97.
| Contrasting effects of two exotic invasive hemipterans on whole‐plant resource allocation in a declining conifer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsFejtbvN&md5=4b417f96f79f31554bf0257239c7301eCAS |
Souto D, Luther T, Chianese B (1995) Past and current status of HWA in eastern and Carolina hemlock stands. In ‘Proceedings of the first hemlock woolly adelgid review’, Charlottesville, VA, USA, 12 October 1995. (Eds SM Salom, TC Tigner, RC Reardon) pp. 9–15. (Forest Health Technology Enterprise Team, USDA Forest Service: Morgantown, West Virginia)
Speer JH (2010) ‘Fundamentals of tree-ring research.’ (University of Arizona Press: Tucson)
Sperry JS, Ikeda T (1997) Xylem cavitation in roots and stems of Douglas-fir and white fir. Tree Physiology 17, 275–280.
| Xylem cavitation in roots and stems of Douglas-fir and white fir.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c%2FlvFClsQ%3D%3D&md5=a242ee713895ed0204dae2ba063b14eeCAS |
Sperry JS, Donnelly JR, Tyree MT (1988) A method for measuring hydraulic conductivity and embolism in xylem. Plant, Cell & Environment 11, 35–40.
| A method for measuring hydraulic conductivity and embolism in xylem.Crossref | GoogleScholarGoogle Scholar |
Sperry JS, Nichols K, Sullivan J, Eastlack S (1994) Xylem embolism in ring-porous, diffuse-porous, and coniferous trees of northern Utah and interior Alaska. Ecology 75, 1736–1752.
| Xylem embolism in ring-porous, diffuse-porous, and coniferous trees of northern Utah and interior Alaska.Crossref | GoogleScholarGoogle Scholar |
Stadler B, Muller T, Orwig D, Cobb R (2005) Hemlock woolly adelgid in New England forests: canopy impacts transforming ecosystem processes and landscapes. Ecosystems 8, 233–247.
| Hemlock woolly adelgid in New England forests: canopy impacts transforming ecosystem processes and landscapes.Crossref | GoogleScholarGoogle Scholar |
Stokes MA, Smiley TL (1996) ‘An introduction to tree-ring dating.’ (University of Arizona Press: Tucson)
Thomas F, Bartels C, Gieger T (2006) Alterations in vessel size in twigs of Quercus robur and Q. petraea upon defoliation and consequences for water transport under drought. IAWA Journal 27, 395–407.
| Alterations in vessel size in twigs of Quercus robur and Q. petraea upon defoliation and consequences for water transport under drought.Crossref | GoogleScholarGoogle Scholar |
Tyree MT, Zimmermann MH (2013) ‘Xylem structure and the ascent of sap.’ (Springer: Berlin)
Wheeler JK, Huggett BA, Tofte AN, Rockwell FE, Holbrook NM (2013) Cutting xylem under tension or supersaturated with gas can generate PLC and the appearance of rapid recovery from embolism. Plant, Cell & Environment 36, 1938–1949.
Wimmer R, Strumia G, Holawe F (2000) Use of false rings in Austrian pine to reconstruct early growing season precipitation. Canadian Journal of Forest Research 30, 1691–1697.
| Use of false rings in Austrian pine to reconstruct early growing season precipitation.Crossref | GoogleScholarGoogle Scholar |
Young RF, Shields KS, Berlyn GP (1995) Hemlock woolly adelgid (Homoptera: Adelgidae): stylet bundle insertion and feeding sites. Annals of the Entomological Society of America 88, 827–835.
| Hemlock woolly adelgid (Homoptera: Adelgidae): stylet bundle insertion and feeding sites.Crossref | GoogleScholarGoogle Scholar |
